The Unfinished Reconstructed Nature of the Last Universal Common Ancestor.

Astrobiology Comparative genomics Early evolution of life on earth

Journal

Journal of molecular evolution

ISSN: 1432-1432

Titre abrégé: J Mol Evol

Pays: Germany

ID NLM: 0360051

Informations de publication

Date de publication:
18 Jul 2024

Historique:

received: 27 01 2024

accepted: 01 07 2024

medline: 19 7 2024

pubmed: 19 7 2024

entrez: 18 7 2024

Statut: aheadofprint

Résumé

The ultimate consequence of Darwin's theory of common descent implies that all life on earth descends ultimately from a common ancestor. Biochemistry and molecular biology now provide sufficient evidence of shared ancestry of all extant life forms. However, the nature of the Last Universal Common Ancestor (LUCA) has been a topic of much debate over the years. This review offers a historical perspective on different attempts to infer LUCA's nature, exploring the debate surrounding its complexity. We further examine how different methodologies identify sets of ancient protein that exhibit only partial overlap. For example, different bioinformatic approaches have identified distinct protein subunits from the ATP synthetase identified as potentially inherited from LUCA. Additionally, we discuss how detailed molecular evolutionary analysis of reverse gyrase has modified previous inferences about an hyperthermophilic LUCA based mainly on automatic bioinformatic pipelines. We conclude by emphasizing the importance of developing a database dedicated to studying genes and proteins traceable back to LUCA and earlier stages of cellular evolution. Such a database would house the most ancient genes on earth.

Identifiants

DOI: 10.1007/s00239-024-10187-8 PMID: 39026043

pubmed: 39026043

doi: 10.1007/s00239-024-10187-8

pii: 10.1007/s00239-024-10187-8

doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

Informations de copyright

Références

Becerra A, Islas S, Leguina JI, Silva E, Lazcano A (1997) Polyphyletic gene losses can bias backtrack characterizations of the cenancestor. J Mol Evol 45:115–118. https://doi.org/10.1007/pl00006209

doi: 10.1007/pl00006209 pubmed: 9236268

Brenner SE, Chothia C, Hubbard TJ (1998) Assessing sequence comparison methods with reliable structurally identified distant evolutionary relationships. Proc Natl Acad Sci USA 95:6073–6078. https://doi.org/10.1073/pnas.95.11.6073

doi: 10.1073/pnas.95.11.6073 pubmed: 9600919 pmcid: 27587

Catchpole RJ, Forterre P (2019) The evolution of reverse gyrase suggests a nonhyperthermophilic last universal common ancestor. Mol Biol Evol 36(12):2737–2747. https://doi.org/10.1093/molbev/msz180

doi: 10.1093/molbev/msz180 pubmed: 31504731 pmcid: 6878951

Chatton E (1925) Pansporella perplexa. Réflexions sur la biologie et la phylogénie des protozoaires. Ann Sci Nat Zool 10e serie, VII:1–84

Chatton E (1938) Titre et travaux scientifique (1906–1937) de Edouard Chatton. Sette, Sottano, Italy

Copeland HF (1938) The kingdoms of organisms. Q Rev Biol 13(383–420):386

Crapitto AJ, Campbell A, Harris AJ, Goldman AD (2022) A consensus view of the proteome of the last universal common ancestor. Ecol Evol 12(6):8930. https://doi.org/10.1002/ece3.8930

doi: 10.1002/ece3.8930

Darwin C (1859) On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. John Murray, London

doi: 10.5962/bhl.title.82303

Dayrat B (2003) The roots of phylogeny: how did Haeckel build his trees? Syst Biol 52:515–527

doi: 10.1080/10635150309310 pubmed: 12857642

Delaye L, Becerra A, Lazcano A (2005) The last common ancestor: what’s in a name? Orig Life Evol Biosph 35:537–554

doi: 10.1007/s11084-005-5760-3 pubmed: 16254691

Doolittle WF (1999) Phylogenetic classification and the universal tree. Science 284:2124–2128. https://doi.org/10.1126/science.284.5423.2124

doi: 10.1126/science.284.5423.2124 pubmed: 10381871

Dose K (1981) Ernst Haeckel’s concept of an evolutionary origin of life. BioSystem 13:253–258

doi: 10.1016/0303-2647(81)90005-8

Eme L, Tamari D, Caceres EF et al (2023) Inference and reconstruction of the heimdallarchaeial ancestry of eukaryotes. Nature 618:992–999. https://doi.org/10.1038/s41586-023-06186-2

doi: 10.1038/s41586-023-06186-2 pubmed: 37316666 pmcid: 10307638

Fitch WM, Upper K (1987) The phylogeny of tRNA sequences provides evidence for ambiguity reduction in the origin of the genetic code. Cold Spring Harb Symp Quant Biol 52:759–767

doi: 10.1101/SQB.1987.052.01.085 pubmed: 3454288

Forterre P (1997) Archaea: what can we learn from their sequences? Review Curr Opin Genet Dev 7:764–770. https://doi.org/10.1016/s0959-437x(97)80038-x

doi: 10.1016/s0959-437x(97)80038-x pubmed: 9468785

Forterre P (2002) A hot story from comparative genomics: reverse gyrase is the only hyperthermophile-specific protein. Trends Genet 18(5):236–237. https://doi.org/10.1016/s0168-9525(02)02650-1

doi: 10.1016/s0168-9525(02)02650-1 pubmed: 12047940

Gogarten JP, Olendzenski L (2002) The Tree/web of life in light of horizontal gene transfer. In: encyclopedia of molecular biology 1962–1964. Wiley, New York, pp 427–435

Gogarten JP, Deamer D (2016) Is LUCA a thermophilic progenote? Nat Microbiol 1:16229. https://doi.org/10.1038/nmicrobiol.2016.229

doi: 10.1038/nmicrobiol.2016.229 pubmed: 27886195

Gogarten JP, Kibak H, Dittrich P, Taiz L, Bowman EJ, Bowman BJ, Manolson MF, Poole RJ, Date T, Oshima T, Konishi J, Denda K, Yoshida M (1989) Evolution of the vacuolar H

doi: 10.1073/pnas.86.17.6661 pubmed: 2528146 pmcid: 297905

Goldman AD, Bernhard TM, Dolzhenko E, Landweber LF (2013) LUCApedia: a database for the study of ancient life. Nucleic Acids Res 41(1):1079–1082. https://doi.org/10.1093/nar/gks1217

doi: 10.1093/nar/gks1217

Gribaldo S, Cammarano P (1998) The root of the universal tree of life inferred from anciently duplicated genes encoding components of the protein-targeting machinery. J Mol Evol 47:508–516. https://doi.org/10.1007/PL00006407

doi: 10.1007/PL00006407 pubmed: 9797401

Haeckel E (1866) Generelle Morphologie der Organismen. Verlag Georg Reimer, Berlin

doi: 10.1515/9783110848281

Harris JK, Kelley ST, Spiegelman GB, Pace NR (2003) The genetic core of the universal ancestor. Genome Res 13:407

doi: 10.1101/gr.652803 pubmed: 12618371 pmcid: 430263

Higgs PG, Lehman N (2015) The RNA world: molecular cooperation at the origins of life. Nat Rev Genet 16(1):7–17

doi: 10.1038/nrg3841 pubmed: 25385129

Iwabe N, Kuma K, Hasegawa M, Osawa S, Miyata T (1989) Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc Natl Acad Sci USA 86:9355–9359. https://doi.org/10.1073/pnas.86.23.9355

doi: 10.1073/pnas.86.23.9355 pubmed: 2531898 pmcid: 298494

Kluyver AJ, Donker HJL (1926) Die Einheit in der Biochemie. Chemie der Zelle und der Gewebe 13:134–190

Koonin EV (2003) Comparative genomics, minimal gene-sets and the last universal common ancestor. Nat Rev Microbiol 1(2):127–136. https://doi.org/10.1038/nrmicro751

doi: 10.1038/nrmicro751 pubmed: 15035042

Koonin EV, Krupovic M, Ishino S, Ishino Y (2020) The replication machinery of LUCA: common origin of DNA replication and transcription. BMC Biol 18(1):61. https://doi.org/10.1186/s12915-020-00800-9

doi: 10.1186/s12915-020-00800-9 pubmed: 32517760 pmcid: 7281927

Kyrpides N, Overbeek R, Ouzounis C (1999) Universal protein families and the functional content of the last universal common ancestor. J Mol Evol 49:413–423. https://doi.org/10.1007/pl00006564

doi: 10.1007/pl00006564 pubmed: 10485999

Lazcano A, Fox GE, Oró J (1992) Life before DNA: the origin and early evolution of early archean cells. In: Mortlock RP (ed) the evolution of metabolic function. CRC Press, Boca Raton, FL, pp 237–295

Leipe DD, Aravind L, Koonin EV (1999) Did DNA replication evolve twice independently? Nucleic Acids Res 27:3389–3401. https://doi.org/10.1093/nar/27.17.3389

doi: 10.1093/nar/27.17.3389 pubmed: 10446225 pmcid: 148579

Line MA (2002) The enigma of the origin of life and its timing. Rev Microbiol 148(1):21–27. https://doi.org/10.1099/00221287-148-1-21

doi: 10.1099/00221287-148-1-21

Mahendrarajah TA, Moody ERR, Schrempf D et al (2023) ATP synthase evolution on a cross-braced dated tree of life. Nat Commun 14:7456. https://doi.org/10.1038/s41467-023-42924-w

doi: 10.1038/s41467-023-42924-w pubmed: 37978174 pmcid: 10656485

Mirkin BG, Fenner TI, Galperin MY, Koonin EV (2003) Algorithms for computing parsimonious evolutionary scenarios for genome evolution, the last universal common ancestor and dominance of horizontal gene transfer in the evolution of prokaryotes. BMC Evol Biol 3:2

doi: 10.1186/1471-2148-3-2 pubmed: 12515582 pmcid: 149225

Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA, Sonnhammer ELL, Tosatto SCE, Paladin L, Raj S, Richardson LJ, Finn RD, Bateman A (2021) Pfam: the protein families database in 2021. Nucleic Acids Res 49(1):D412–D419. https://doi.org/10.1093/nar/gkaa913

doi: 10.1093/nar/gkaa913 pubmed: 33125078

Mushegian AR, Koonin EV (1996) A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proc Natl Acad Sci USA 93(19):10268–10273. https://doi.org/10.1073/pnas.93.19.10268

doi: 10.1073/pnas.93.19.10268 pubmed: 8816789 pmcid: 38373

Orengo CA, Thornton JM (2005) Protein families and their evolution—a structural perspective. Annu Rev Biochem 74:867–900. https://doi.org/10.1146/annurev.biochem.74.082803.133029

doi: 10.1146/annurev.biochem.74.082803.133029 pubmed: 15954844

Ouzounis CA, Kunin V, Darzentas N, Goldovsky L (2006) A minimal estimate for the gene content of the last universal common ancestor–exobiology from a terrestrial perspective. Res Microbiol 157:57–68. https://doi.org/10.1016/j.resmic.2005.06.015

doi: 10.1016/j.resmic.2005.06.015 pubmed: 16431085

Prosdocimi F, José MV, de Farias ST (2019) The First Universal Common Ancestor (FUCA) as the earliest ancestor of LUCA’s (Last UCA) lineage. In: Pontarotti P (ed) Evolution, origin of life, concepts and methods. Springer, Cham

Ranea JAG, Sillero A, Thornton JM, Orengo CA (2006) Protein superfamily evolution and the last universal common ancestor (LUCA). J Mol Evol 63:513–525. https://doi.org/10.1007/s00239-005-0289-7

doi: 10.1007/s00239-005-0289-7 pubmed: 17021929

Raymann K, Brochier-Armanet C, Gribaldo S (2015) The two-domain tree of life is linked to a new root for the archaea. Proc Natl Acad Sci USA 112:6670–6675. https://doi.org/10.1073/pnas.1420858112

doi: 10.1073/pnas.1420858112 pubmed: 25964353 pmcid: 4450401

Sapp J (2005) The prokaryote–eukaryote dichotomy: meanings and mythology. Microbiol Mol Biol Rev 69(2):292–305. https://doi.org/10.1128/MMBR.69.2.292-305.2005

doi: 10.1128/MMBR.69.2.292-305.2005 pubmed: 15944457 pmcid: 1197417

Sauguet L (2019) The extended “two-barrel” polymerases superfamily: structure, function and evolution. J Mol Biol 431:4167–4183

doi: 10.1016/j.jmb.2019.05.017 pubmed: 31103775

Singleton R, Singleton DR (2017) Remembering our forebears: Albert Jan Kluyver and the unity of life. J Hist Biol 50:169–218. https://doi.org/10.1007/s10739-016-9438-7

doi: 10.1007/s10739-016-9438-7 pubmed: 26869464

Srinvasan V, Morowitz HJ (2009) The canonical network of autotrophic intermediary metabolism: minimal metabolome of a reductive chemoautotroph. Biol Bull 216:126–130

doi: 10.1086/BBLv216n2p126

Stanier RY, van Niel CB (1941) The main outlines of bacterial classification. J Bacteriol 42:437–466

doi: 10.1128/jb.42.4.437-466.1941 pubmed: 16560462 pmcid: 374769

Stanier RY, van Niel CB (1962) The concept of a bacterium. Arch Microbiol 42:17–35

Wang M, Yafremava LS, Caetano-Anollés D, Mittenthal JE, Caetano-Anollés G (2007) Reductive evolution of architectural repertoires in proteomes and the birth of the tripartite world. Genome Res 17:1572–1585

doi: 10.1101/gr.6454307 pubmed: 17908824 pmcid: 2045140

Weiss MC, Sousa FL, Mrnjavac N, Neukirchen S, Roettger M, Nelson-Sathi S, Martin WF (2016a) The physiology and habitat of the last universal common ancestor. Nat Microbiol 1(9):16116. https://doi.org/10.1038/nmicrobiol.2016.116

doi: 10.1038/nmicrobiol.2016.116 pubmed: 27562259

Weiss MC, Neukirchen S, Roettger M, Mrnjavac N, Nelson-Sathi S, Martin WF, Sousa FL (2016b) Reply to ‘Is LUCA a thermophilic progenote?’ Nat Microbiol 1:16230. https://doi.org/10.1038/nmicrobiol.2016.230

doi: 10.1038/nmicrobiol.2016.230 pubmed: 27886196

Whittaker RH (1996) New concepts of kingdoms of organisms. Science 163:150–160

doi: 10.1126/science.163.3863.150

Williams T, Foster P, Cox C et al (2013) An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504:231–236. https://doi.org/10.1038/nature12779

doi: 10.1038/nature12779 pubmed: 24336283

Woese C (1998) The universal ancestor. Proc Natl Acad Sci USA 95:6854–6859. https://doi.org/10.1073/pnas.95.12.6854

doi: 10.1073/pnas.95.12.6854 pubmed: 9618502 pmcid: 22660

Woese CR, Fox GE (1977a) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74:5088–5090. https://doi.org/10.1073/pnas.74.11.5088

doi: 10.1073/pnas.74.11.5088 pubmed: 270744 pmcid: 432104

Woese CR, Fox GE (1977b) The concept of cellular evolution. J Mol Evol 10:1–6. https://doi.org/10.1007/BF01796132

doi: 10.1007/BF01796132 pubmed: 903983

Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains archaea, bacteria, and eucarya. Proc Natl Acad Sci USA 87:4576–4579. https://doi.org/10.1073/pnas.87.12.4576

doi: 10.1073/pnas.87.12.4576 pubmed: 2112744 pmcid: 54159

Yang S, Doolittle RF, Bourne PE (2005) Phylogeny determined by protein domain content. Proc Natl Acad Sci USA 102:373–378

doi: 10.1073/pnas.0408810102 pubmed: 15630082 pmcid: 540256